As a winger, Pleat represented England at schoolboy level. His first club as a senior player was Nottingham Forest (1962–64), which was his local club. From there he moved on to Luton Town (1964–67), Shrewsbury Town (1967–68) and Exeter City (1968–70), where he once played outside left against the team that he was later to manage, Tottenham Hotspur. His playing career ended with a stint at Peterborough United (1970–71), after which he turned to coaching and management.[4]

From there he joined the coaching staff at Luton Town. In January 1978 he was appointed manager of the club. During his nine years as manager of Luton Town the side were promoted from the Football League Second Division to the First Division and gained a reputation for playing attacking and attractive football, peaking at ninth place in the league in 1986, his final year in charge. A number of players in Pleat's team would receive international recognition, including defender Mal Donaghy (Northern Ireland), midfielder Ricky Hill and forwards Brian Stein, Paul Walsh and Mick Harford (all England).

Luton came close to reaching the FA Cup final in 1985 under Pleat. They were beaten 2–1 by Everton in the semi-final in extra time at Villa Park. Luton also lost in the quarter-final against Everton the following year.[6][7] Although Luton did not manage to reach a Cup final during Pleat's time in charge, the team that won the 1988 Littlewoods Cup under Ray Harford, beating Arsenal 3–2 in the final, was largely Pleat's team of the early and mid-1980s.[4] (For more information, see History of Luton Town F.C. (1970–present))

In May 1986, Pleat was appointed manager of Tottenham Hotspur, one of the biggest clubs in England. He brought along with him from Luton Mitchell Thomas. His earliest changes at the club were to bring in Nico Claesen and Richard Gough, the latter of whom he paired with Gary Mabbutt in defence, moving Paul Allen into midfield.[4] During his only full season as manager, Tottenham Hotspur reached third place in the First Division, reached the FA Cup final, and the semi-final of the Football League Cup in the 1986–87 season. Glenn Moore, writing in The Independent in 1995, described the play during Pleat's stint as manager of Spurs as "some of the best attacking football of the last two decades". During this season, he played with just one striker - Clive Allen, who scored a highly impressive total of 49 goals in all competitions. They had been in serious contention for all three major English trophies that season, although they ended the season without winning any of them.[8]

Pleat's employment as manager of Tottenham came to an end in October 1987 when he was dismissed due to "disclosures about his private life".[9] Newspaper revelations that Pleat had been cautioned by police three times for kerb-crawling created publicity that forced him to leave Spurs.[10] The board of Tottenham Hotspur were also keen to bring Terry Venables to the club as manager, since he had also become available.[8]

Pleat made a quick return to management with Leicester City, who had just been relegated from the First Division, and lasted more than three years at Filbert Street before he was dismissed in January 1991, with Leicester still yet to win promotion to the First Division and looking more likely to be relegated to the Third Division, never finishing above mid table while Pleat was in charge.[11] He returned to Luton Town in June 1991 for a second spell as manager of the club. They were relegated at the end of his first season back at Kenilworth Road, missing out on a place in the new FA Premier League, but the club's board kept faith in him. Despite dismal form in the new Division One, they did reach the FA Cup semi-final in 1994, losing 2-0 to Chelsea.[12]

The club won its first four fixtures of the 1996–97 season, against Aston Villa, Leeds United, Newcastle United and Leicester City, earning Pleat the Premier League Manager of the Month for August 1996 as the Owls topped the Premier League. However, they failed to keep up this good form and any hopes of a league title triumph were soon forgotten, and by Christmas even a UEFA Cup place was looking unlikely. They eventually finished seventh in the final table. They started the following season dismally and Pleat was sacked in November 1997 with relegation looking a real possibility.

He returned to Tottenham Hotspur as Director of Football in 1998.[9][13] In September 2003, after the sacking of Glenn Hoddle, he took over as caretaker manager for Tottenham Hotspur,[13][14] a position that he held until the end of the season.[9][15] This was the third of three occasions in which he had been caretaker manager for Tottenham Hotspur.[9] He had previously been caretaker manager in 1998, before George Graham became manager, during which time the team had four wins, two draws, and one defeat.[5]

In August 2006, Pleat returned to his first and home club, Nottingham Forest, this time as a football consultant, a job which included advising new Forest manager Colin Calderwood and scouting potential signings.[16] In August 2009, Pleat had more time available, and was in discussion with the Forest chief executive about expanding his role.[17][18] On 28 September 2011, Pleat left his role, following the disbanding of the much criticized acquisition panel.[19]

Pleat has written a regular column for The Guardian newspaper since 2004, primarily exploring the tactical side of recent matches,[21] and contributes articles to the Daily Mail.[22] He spent a number of years working for ITV as a commentator, but left in August 2009. He has been a regular co-commentator on Radio 5 Live and now contributes a regular column for BackPass magazine.[23]

Pleat has worked as a co-commentator for ESPN UK broadcasts. He has also commentated for Premier League Productions, which provides the world feed commentary. Pleat is currently working for Al Jazeera Sport.[citation needed]